Beyond basic characterization and omics: Immunomodulatory roles of platelet‐derived extracellular vesicles unveiled by functional testing
Abstract Renowned for their role in haemostasis and thrombosis, platelets are also increasingly recognized for their contribution in innate immunity, immunothrombosis and inflammatory diseases. Platelets express a wide range of receptors, which allows them to reach a variety of activation endpoints...
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Wiley
2024-10-01
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| Series: | Journal of Extracellular Vesicles |
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| Online Access: | https://doi.org/10.1002/jev2.12513 |
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| author | Mari Palviainen Johanna Puutio Rikke Halse Østergaard Johannes A. Eble Katariina Maaninka Umar Butt Joseph Ndika Otto K. Kari Masood Kamali‐Moghaddam Kasper Kjaer‐Sorensen Claus Oxvig Ana M. Aransay Juan M. Falcon‐Perez Antonio Federico Dario Greco Saara Laitinen Yuya Hayashi Pia R.‐M. Siljander |
| author_facet | Mari Palviainen Johanna Puutio Rikke Halse Østergaard Johannes A. Eble Katariina Maaninka Umar Butt Joseph Ndika Otto K. Kari Masood Kamali‐Moghaddam Kasper Kjaer‐Sorensen Claus Oxvig Ana M. Aransay Juan M. Falcon‐Perez Antonio Federico Dario Greco Saara Laitinen Yuya Hayashi Pia R.‐M. Siljander |
| author_sort | Mari Palviainen |
| collection | DOAJ |
| description | Abstract Renowned for their role in haemostasis and thrombosis, platelets are also increasingly recognized for their contribution in innate immunity, immunothrombosis and inflammatory diseases. Platelets express a wide range of receptors, which allows them to reach a variety of activation endpoints and grants them immunomodulatory functions. Activated platelets release extracellular vesicles (PEVs), whose formation and molecular cargo has been shown to depend on receptor‐mediated activation and environmental cues. This study compared the immunomodulatory profiles of PEVs generated via activation of platelets by different receptors, glycoprotein VI, C‐type lectin‐like receptor 2 and combining all thrombin‐collagen receptors. Functional assays in vivo in zebrafish and in vitro in human macrophages highlighted distinct homing and secretory responses triggered by the PEVs. In contrast, omics analyses of protein and miRNA cargo combined with physicochemical particle characterization found only subtle differences between the activated PEV types, which were insufficient to predict their different immunomodulatory functions. In contrast, constitutively released PEVs, formed in the absence of an exogenous activator, displayed a distinct immunomodulatory profile from the receptor‐induced PEVs. Our findings underscore that PEVs are tunable through receptor‐mediated activation. To truly comprehend their role(s) in mediating platelet functions among immune cells, conducting functional assays is imperative. |
| format | Article |
| id | doaj-art-d1bacf0104064fd49990f7e4e0293c8c |
| institution | OA Journals |
| issn | 2001-3078 |
| language | English |
| publishDate | 2024-10-01 |
| publisher | Wiley |
| record_format | Article |
| series | Journal of Extracellular Vesicles |
| spelling | doaj-art-d1bacf0104064fd49990f7e4e0293c8c2025-08-20T01:57:59ZengWileyJournal of Extracellular Vesicles2001-30782024-10-011310n/an/a10.1002/jev2.12513Beyond basic characterization and omics: Immunomodulatory roles of platelet‐derived extracellular vesicles unveiled by functional testingMari Palviainen0Johanna Puutio1Rikke Halse Østergaard2Johannes A. Eble3Katariina Maaninka4Umar Butt5Joseph Ndika6Otto K. Kari7Masood Kamali‐Moghaddam8Kasper Kjaer‐Sorensen9Claus Oxvig10Ana M. Aransay11Juan M. Falcon‐Perez12Antonio Federico13Dario Greco14Saara Laitinen15Yuya Hayashi16Pia R.‐M. Siljander17EV Group, Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, and CURED, Drug Research Program, Faculty of Pharmacy University of Helsinki Helsinki FinlandEV Group, Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, and CURED, Drug Research Program, Faculty of Pharmacy University of Helsinki Helsinki FinlandDepartment of Molecular Biology and GeneticsAarhus UniversityAarhusDenmarkInstitute of Physiological Chemistry and PathobiochemistryUniversity of MünsterMünsterGermanyEV Group, Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, and CURED, Drug Research Program, Faculty of Pharmacy University of Helsinki Helsinki FinlandEV Group, Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, and CURED, Drug Research Program, Faculty of Pharmacy University of Helsinki Helsinki FinlandDrug Research Program, Faculty of PharmacyUniversity of HelsinkiHelsinkiFinlandDrug Research Program, Faculty of PharmacyUniversity of HelsinkiHelsinkiFinlandDepartment of Immunology, Genetics and Pathology, Science for Life LaboratoryUppsala UniversityUppsalaSwedenDepartment of Molecular Biology and GeneticsAarhus UniversityAarhusDenmarkDepartment of Molecular Biology and GeneticsAarhus UniversityAarhusDenmarkGenome Analysis Platform, Center for Cooperative Research in BiosciencesBasque Research and Technology Alliance (BRTA)MendaroSpainCentro de Investigación Biomédica en Red de Enfermedades Hepáticas Y Digestivas (CIBERehd)MadridSpainFinnish Hub for Development and Validation of Integrated Approaches (FHAIVE); Faculty of Medicine and Health TechnologyTampere UniversityTampereFinlandFinnish Hub for Development and Validation of Integrated Approaches (FHAIVE); Faculty of Medicine and Health TechnologyTampere UniversityTampereFinlandResearch and DevelopmentFinnish Red Cross Blood Service (FRCBS)Helsinki FinlandDepartment of Molecular Biology and GeneticsAarhus UniversityAarhusDenmarkEV Group, Molecular and Integrative Biosciences Research Programme, Faculty of Biological and Environmental Sciences, and CURED, Drug Research Program, Faculty of Pharmacy University of Helsinki Helsinki FinlandAbstract Renowned for their role in haemostasis and thrombosis, platelets are also increasingly recognized for their contribution in innate immunity, immunothrombosis and inflammatory diseases. Platelets express a wide range of receptors, which allows them to reach a variety of activation endpoints and grants them immunomodulatory functions. Activated platelets release extracellular vesicles (PEVs), whose formation and molecular cargo has been shown to depend on receptor‐mediated activation and environmental cues. This study compared the immunomodulatory profiles of PEVs generated via activation of platelets by different receptors, glycoprotein VI, C‐type lectin‐like receptor 2 and combining all thrombin‐collagen receptors. Functional assays in vivo in zebrafish and in vitro in human macrophages highlighted distinct homing and secretory responses triggered by the PEVs. In contrast, omics analyses of protein and miRNA cargo combined with physicochemical particle characterization found only subtle differences between the activated PEV types, which were insufficient to predict their different immunomodulatory functions. In contrast, constitutively released PEVs, formed in the absence of an exogenous activator, displayed a distinct immunomodulatory profile from the receptor‐induced PEVs. Our findings underscore that PEVs are tunable through receptor‐mediated activation. To truly comprehend their role(s) in mediating platelet functions among immune cells, conducting functional assays is imperative.https://doi.org/10.1002/jev2.12513extracellular vesiclesfunctional assaysimmunomodulatoryinflammationinnate immunitymacrophages |
| spellingShingle | Mari Palviainen Johanna Puutio Rikke Halse Østergaard Johannes A. Eble Katariina Maaninka Umar Butt Joseph Ndika Otto K. Kari Masood Kamali‐Moghaddam Kasper Kjaer‐Sorensen Claus Oxvig Ana M. Aransay Juan M. Falcon‐Perez Antonio Federico Dario Greco Saara Laitinen Yuya Hayashi Pia R.‐M. Siljander Beyond basic characterization and omics: Immunomodulatory roles of platelet‐derived extracellular vesicles unveiled by functional testing Journal of Extracellular Vesicles extracellular vesicles functional assays immunomodulatory inflammation innate immunity macrophages |
| title | Beyond basic characterization and omics: Immunomodulatory roles of platelet‐derived extracellular vesicles unveiled by functional testing |
| title_full | Beyond basic characterization and omics: Immunomodulatory roles of platelet‐derived extracellular vesicles unveiled by functional testing |
| title_fullStr | Beyond basic characterization and omics: Immunomodulatory roles of platelet‐derived extracellular vesicles unveiled by functional testing |
| title_full_unstemmed | Beyond basic characterization and omics: Immunomodulatory roles of platelet‐derived extracellular vesicles unveiled by functional testing |
| title_short | Beyond basic characterization and omics: Immunomodulatory roles of platelet‐derived extracellular vesicles unveiled by functional testing |
| title_sort | beyond basic characterization and omics immunomodulatory roles of platelet derived extracellular vesicles unveiled by functional testing |
| topic | extracellular vesicles functional assays immunomodulatory inflammation innate immunity macrophages |
| url | https://doi.org/10.1002/jev2.12513 |
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